AI-generated definition based on ‘Quantitative and analytical tools to analyze the spatiotemporal population dynamics of microbial consortia’, Current Opinion in Biotechnology, August 2022:

The Red Queen hypothesis refers to the idea that a constant rate of extinction persists in a community, independent of the duration of a species’ existence, driven by interspecies relationships where beneficial mutations in one species can negatively impact others.

Encyclopedia of Ecology (second ed.), 2008:

The term is derived from Lewis Carroll’s Through the Looking Glass, where the Red Queen informs Alice that “here, you see, it takes all the running you can do to keep in the same place.” Thus, with organisms, it may require multitudes of evolutionary adjustments just to keep from going extinct.

The Red Queen hypothesis serves as a primary explanation for the evolution of sexual reproduction. As parasites (or other selective agents) become specialized on common host genotypes, frequency-dependent selection favors sexual reproduction (i.e., recombination) in host populations (which produces novel genotypes, increasing the rate of adaptation). The Red Queen hypothesis also describes how coevolution can produce extinction probabilities that are relatively constant over millions of years, which is consistent with much of the fossil record.

Also read: ‘Sexual reproduction as an adaptation to resist parasites (a review).’, Proceedings of the National Academy of Sciences, May 1, 1990.

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In nature, scientists have found that even very similar strains of bacteria constantly appear and disappear even when their environment doesn’t seem to change much. This is called continual turnover. In a new study in PRX Life, Aditya Mahadevan and Daniel Fisher of Stanford University make sense of how this ongoing change happens, even without big differences between species or dramatic changes in the environment. Their jumping-off point is the red queen hypothesis.

While the hypothesis has usually been used to talk about ‘arms races’, like between hosts and parasites, the new study asked: can continuous red queen evolution also happen in communities where different species or strains overlap a lot in what they do and where there aren’t obvious teams fighting each other?

Mahadevan and Fisher built mathematical models to mimic how communities of microbes evolve over time. These models allowed the duo to simulate what would happen if a population started with just one microbial strain and over time new strains appeared due to random changes in their genes (i.e. mutations). Some of these new strains could invade other species’ resources and survive while others are forced to extinction.

The models focused especially on ecological interactions, meaning how strains or species affected each other’s survival based on how they competed for the same food.

When they ran the models, the duo found that even when there were no clear teams (like host v. parasite), communities could enter a red queen phase. The overall number of coexisting strains stayed roughly constant, but which strains were present keeps changing, like a continuous evolutionary game of musical chairs.

The continual turnover happened most robustly when strains interacted in a non-reciprocal way. As ICTS biological physicist Akshit Goyal put it in Physics:

… almost every attempt to model evolving ecological communities ran into the same problem: One organism, dubbed a Darwinian monster, evolves to be good at everything, killing diversity and collapsing the community. Theorists circumvented this outcome by imposing metabolic trade-offs, essentially declaring that no species could excel at everything. But that approach felt like cheating because the trade-offs in the models needed to be unreasonably strict. Moreover, for mathematical convenience, previous models assumed that ecological interactions between species were reciprocal: Species A affects species B in exactly the same way that B affects A. However, when interactions are reciprocal, community evolution ends up resembling the misleading fixed fitness landscape. Evolution is fast at first but eventually slows down and stops instead of going on endlessly.

Mahadevan and Fisher solved this puzzle by focusing on a previously neglected but ubiquitous aspect of ecological interactions: nonreciprocity. This feature occurs when the way species A affects species B differs from the way B affects A—for example, when two species compete for the same nutrient, but the competition harms one species more than the other

Next, despite the continual turnover, there was a cap on the number of strains that could coexist. This depended on the number of different resources available and how strains interacted, but as new strains invaded others, some old ones had to go extinct, keeping diversity within limits.

If some strains started off much better (i.e. with higher fitness), over time the evolving competition narrowed these differences and only strains with similar overall abilities managed to stick around.

Finally, if the system got close to being perfectly reciprocal, the dynamics could shift to an oligarch phase in which a few strains dominated most of the population and continual turnover slowed considerably.

Taken together, the study’s main conclusion is that there doesn’t need to be a constant or elaborate ‘arms race’ between predator and prey or dramatic environmental changes to keep evolution going in bacterial communities. Such evolution can arise naturally when species or strains interact asymmetrically as they compete for resources.

Featured image: “Now, here, you see, it takes all the running you can do, to keep in the same place.” Credit: Public domain.